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International Council ror the .
Exploration of the Sea
StatutOl-y Meeting~.
C.M. 19931F:27
Mariculture Committee
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Introductions of exotic species associated with Pacific oyster transfers
from France to Ireland.
D. Minchin, C.B. Duggan, J.M.C. Holmes* & S. Neiland.
Fisheries Research Centre, Department of the Marine, Abbotstown,
Dublin 15, Ireland.
:' * Natural History Division, National Museum of Ireland, Kildare Street,
. Dublin 2, Ireland.
•
SUMMARY
Following the implementation of EC Council Directive 91/67/EEC, the free
movement of trade in shellfish commenced in January 1993. This
Directive permitted transfers of Pacific oysters, Crassostrea gigas, which
previous Irish legislation had controlled. Importations from France took
place from January 1993. All importations were certified as being free
from Bonamia and Martelia and also free from other species. Sampies
from consignments revealed the presence of Mytilicola orientalis, Myicola
ostrea, Crepidula fornicata, Ostrea edulis and Mytilus edulis. The
biomass of the importations and the frequency of M. orientalis and M.
ostrea in these consignments suggest that they may become established
in Irish waters and that there was a risk, albeit smalI, of introducing
pathogens associated with these species in Irish relaying areas. Oysters
sourced from Marennes-Oleron had other exotic species present.
INTRODUCTION
Until the end of 1992 Ireland had a policy of banning all mollusc
importations except under licence. Transfers from inspected sites in
Norway, Great Britain and Guernsey have been permitted. This policy
rela~es to Ireland being an Island and so in a position to exclude pests
as weil as invertebrate and fish diseases. However some introductions
are already known as a result of shellfish transfers, such as Crepidula
fornicata (Minchin et al., in press - no live populations or specimens of
.
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this species in Ireland are known to exist sin'ce 1963), Calyptraea
chinensis (Minchin et a/., 1987) and shell disease of the oyster Ostrea
edulis (Duggan - internal report, 1963). These introductions tagether
with outbreak of various oyster dis~ases in Europe led to the strict
control of all importations to Ireland, despite wh ich an illegal importation
of the oyster Ostrea edulis lead to the establishment of Bonamia ostrea
disease in Cork Haroour, Gaiway Bay and possibly in Clew Bay. Once
the disease was identified~ restrietions on ttie transfer of oysters
thoughout Ireland were imposed, movements being permissable only
under Iicence. The disease-free status of Ireland was compromised by
Bonamia and shellfish exports from Ireland were impeded. The
implementation of the EC Directive on trade in shellfish is Iikely to
compromise shellfish cultivation in Ireland furttler with the eventual
establishment of non-native flora and fauna which are Iikely to interact
with Irish marine communities.
Exotic species such as Crassostrea gigas, Ruditapes semidecussataj
Haliotus discus hannai, Ha/iotus tubercu/ata, had all been successfully
introduced into Ireland using the ICES Code of Practice so that the
introduction of pests, parasites and diseases were avoided. In all cases
introductions were made through quarantine. The most recent
introduction of the Japanese scallop, Patinopecten yessoensis (in 1990)
was under tighter controls as the ICES Code of Practice had been
updated. Future intended introductions of exotic commercial species will
continue to be subject to the tull protocol~o! the currerit iCES Code of
Practice.
METHODS
Oysters imported trom France were selected either trom oyster bags
removed trom different parts ot the consignment during unloadingi or as
sampies received trom growers or from trestles on the shore. Oysters
wereweighed and measured and the trequency of associated species .
tound in the gut (Mytilico/a orienta/is Mori, 1935 identitied using Ho &
Kim, 1992), or attached to the gills or within the shell cavity (Myico/a
ostreae Hoshima & Sugiura, 1953 identified using Ho & Kim 1991) cr on
the shell surtace (Crepidu/a fornicata (L.) and Ostrea edu/is L.). Other
associated organisms were also removed. Sampies were obtained trom
different regions within the country to wh ich consignments were known
to have been dispatched.
Dinoflagellate cysts were found in sediment within the valves of dead
oysters associated with oysters transterred in January 1993 and are
discussed elsewhere (O'Mahony, 1993). These had been kept in a cold
room for same weeks prior to examination .
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RESULTS
The first known importation was to Cariingfora on 23 January 1993, of
half grown oysters from the Marennes-Oleron region in Freince. Their
conaition was very poor, they heia translucent flesh, a very reduced
digestive gland and many were gapirig and had long narrow shells.
Subsequent consignments were of marginally better quality. All sampies
demonstrated varying frequencies of associated exotics (Table 1). The
regions where oyster reiayings have taken place are shown in Figure 1.
Up to 10M. orientalis were found in the gut of an oyster. When present
in m.imbors these produced a pea-size swelling of the rectum and the
female copepods were easily seen through the Iining of the gut.
,
Specimeris were orange/pink in coloratiori. Infestation frequencies varied
greatly between sampies. Those iriüoduced to Carlingforrl in January had
an irifestation of 7.3% which haa reduced to 2.3% in March in a sampie
of the same importation; the decline in the frequency corresponded with
.an increase in oyster mortality over this period. Egg strings were found in
',samples taken in January and March. This species was found within
:, Pacific oysters from wild settlements in t~e Oleron arid Archachon
'regions but also from nursery-raised spat, with adult female copepods
and attached e9g strings being found in oysters fram ca 1g.
Myicola ostreae was found either adhering to the gills, free on tlle gills or
within the manile cavity. Where they wore found on tlle cream coloured
gills, they were often associated with a small light oval patch; witl, up to
tllree being taken from a single oyster.
Two Crepidula fornicata were found attached to the shells of oysters
o,riginating from Marennes-Oleron. These were both males of 6 arid 8mm
shell length.
The surface of many of the imported oysters haa an attached serpulid
Pomatoceros sp. (Polychaeta). Sediment fram within oysters contained
specimens of Tenibella lapidaria (Polychaeta), both previously unreported
from Irish weiters.
Marine aigae associated with oyster imjJortations were not examiried.
DISCUSSION
Exotic species are known to spread by ~he movement of shelifish, in
particular with transfers involving oysters: Expansion of the movements
of oysters following the EC Council Directive 91/67/EEC which concerns
the trade in living aquaculture proaucts, ~i11 merin that there will most
certainly be an expansion of the ranges of vai"ious species of flora and
fauna associated with the shellfish transfers. The ICES Code of Practice
for the Introduction and Transfers of species considors the transfer, not
_
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only of the organism under transfer, but also of associated species. As
the introductions of many shellfish species to coritinental Europe took
place at a time when the ICES Code of Practice had not been fully
formed, a number of species that fall into the category of pest or fouling
species became established including M. orientalis and Hydroides elegans
in France (His et al., 1978).
Many species survived the transfer from the Pacific to Fra~ce which
would have taken same days, so they are likely to survive the shorter
transfer from France to Ireland.
The presence of Ostrea edulis and Mytilus edulis in. consignments is of
cancern. Although not quantified musseis, M. edulis, have appeared in
all consignments of half-grown oysters. 80th O. edulis and M. edulis are
known vectors of Martelia refringens (Tige & Raboun, 1976; Camps et
al., 1975). In the case of the protozoan Bonamia ostreae the flat oyster,
..9. edulis, is a vector. Pathogens have been identified in Japanese Pacific
i oysters, from whence the French introductions came. These include a
:,haplosporidian (Friedman, 1991) and a herpes-Iike virus in Pacific oyster
.' larvae reared in French oyster hatcheries (Nicholas et 81., 1992). There is
cancern that these may spread to oyster culture areas. This rccent
information questions tf:1e use of even hatchery-reared Pacific oysters
being suitable for transfer for cultivation within uriinfected areas.
M. orientalis was not known in Irish waters until prior to the transfer of
Pacific oysters from France in 1993. This parasite is known to cause
damage to the lining of the gut of the oys~er C. gigas, the mucosa being
destroyed with penetration into the underJying connective tissue (Sparks,
1962), but Bernard (1969) was not able to show histological damage in
his study. Grizel (1985) refers to its ab!J~ty to cause a reduction in
condition index, and in severe cases to cause mortality. His et al.
(1978), record mortalities of up to 50% in oyster growing areas in
France. Chew et al., (1965) noted that infested oysters in the north-east
Pacific were not as weil conditioned and Odlaug (1946) recorded that
infested oysters lost condition more rapidly following spawning. DeslousPaoli (1981) in his study concludes that the size of the hast is important,
having found M. orientalis in six-month-old Pacific oysters. He claims that
in cases where three female specimens appear in a hast there is a
significant decrease of rates of carbohYdr~te and glycogen production,
presumably infestations greater than this'~liave
",.greater demands on the
hast.
One method of control proposed by Grizel is the complete prevention of
transfer (Grizel, 1985). More recently, recognising that Mytilicola
intestinalis can cause problems for musseis, he rind others (Blateau et al.,
1992) have examined treatments to eliminate infestation levels using
dichlorvos.
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The cr"itical numbers of M. orientalis required to establish a population
may depEmd on the local conditions to which the animals have been
introduced. Enclosed inlets with poor to moderate tidal flushing are
probably more likeiy to dEwelop.local populations. It is considered that
Carlingford Lough may be suitable for expansion of this parasitic copepod
which is known to infest oysters and musseis and trochid snaiis. Almost
50 tonnes of oysters with a 3-1 2 % infestation rate have already been
relayed in Cadingford. Transfers of nursery-reared spat, are also capable
of holding ovigerous female copepods. Eggs of these copepods may
develop within smaller oysters once swallowed. It may be necessary to
consider filtered supplies of seawater in order to avoid infestation of
oysters in hatcheries. Ovigerous females were present in January and
Fehruary; indicnting that in France reproduction may take plnce nll year.
in Bi-itish Cohjmbia Bernard (1969) showed that reproduction takes place
from June to late August and t~nt the main population of the copepod
was confined to Ladysmith Harbour where the .original introductions of
Pncific oysters took place. He reports that the larval stages of this
species are short nnd ttley do not travel far, and lnterestingly states that
•oysters rind musseis raised above the substrate are not infested. This last
~ statement wouid not appear to be borne out in the French experience
'because imported half-grown oysters had previously been cultivatcid on
trestles.
The related species Mytilicola intestinalis Steuer is known in Irish waters
only from Galway Bay and the coastline of Co Cork (Crowley, 1972),
but not from Carlingford Lough (Crowley, 1972) where niusseis were
again examined in 1993 together with clams and oysters~ Korringa
(1951) recorded it in Dutch waters as tlaving an adverse effect causing
mortality in some cases. Theisen (1987) noted that it has a marked
effect on concÜtion in the mussei, Mytilus edulis L., but although Davey
(1989) found some slight reductions of musseI growth in his studies in.
Cornwall, England, he conciudedthat M. edulis had no harmful impact on
musseIs and that the species had features in common with a commensal.
Introductions of Paciflc oysters wittl M. orientalis must have
consequences for other marine populations. Ttle species is known to
.
occur in val-ious oysters, musseis, clams ~md trochid and cither snails and
to-date there have boen no quantified studies of its effect on the'se
species. It is known to have taken up new molluscan hosts in British
Columbia (Bernard, 1969).
Myicola ostreae is a poecilostome copepod previously known from
C.gigas in Japan and Korea, and more recently in France following the .
1970's direct oyster transfers. The family, Myicolidae are mainly found
on the gilis of marine bivalve molluscs. This species is also known to
occur within Ostrea edulis in the Baissin d' Arcachon (His, 1977).
·.
Thore is sufficient evidence to suggest that the introduction cif Crepidula
fornicata can result in serious modification of trophic relationships within
muddy estuaries and bays, areas where oysters and musseis are often
cultivated. Successive introductions of Gonsignments containing small
and relatively incorispicuous individuals, .as found in this study, could
lead to the establishment of breeding populations. Since the 1920's
(Spicer,1923) Ireland has been weil aware of the possibility of the
introduction of C. fornicata and measures to prevent its importation
were a feature of the licensing system controlling all oyster impo'rtations
at that time. It does appear that, despite screening, some small
populations were transferred to Clevil and Kenmare Bays following ,
separate and unsustained importations of oysters (0. edulis) for laying,
but fortunately these did not survive. Should populations of C. fornicata
become established there may be significarit changes in:
(a) trophic competition,
(b) changes in the texture of the sea bed, and
" (c) modification of the benthos.
;In France the abundance of this species in certain bays is such that
! dredging of the sea-bed for their removal is sometimes necessary to
enable management of growth of oysters vilithin the same bay (Anon,
1985). In the Grariville area of Normandy the population has increased
from 150,000t in 1985 to 750,000t in 1992 (Anon,.1993).
Sargassum muticum is widely distributed within oyster growing areas in
France. Transfers of germlings of this phaeophyte on oysters are a
poteritial risk with oyster importations. S. muticum exterided its range to
the North-east Pacific at the same time aOs oyster importations and it is
Iikely that they were transferred with oysters. More recently Critchley &
Dijkema (1984) demonstrated a transfer of S. muticum on native oysters
Ostrea edulis from The Solent in England to Yeseke, The Netherlands.
This plant can be easily transferred from a small size as has been
determined in experiments by Yamauchi (1984). Being a monoecious
species a single plant can result in the development of a population, and
can become mature within a year. Introductions of this species to Ireland
are not only possible but probable with sustained transfers of oysters.
According to Scagel (1956) Canadian oyster fishermen have difficulty in
observing their stock beneath the extensive stands of S. muticum. 'The
plants are buoyant and when attached to oysters can cause them to be
transferred elsewhere. Critchley & Dijkema (1984) make an appeal at the
end of their paper ..... A call is made for the rigid application of existing
quarantine procedures regarding the movement of shellfish and the
establishment of an international body (perhaps as part of the European
Economic Community) to both administer and enforce these
regulations" ...
The transfers of shellfish species in the course of trade result in the
transfer and establishment of exotic species. The movements of
..
organisms between different biological prayinces can result in
unexpected consequences • Examples of this include: the zebra mussei
Dreissena polymorpha from the Black Sea to The Great Lakes (Snyder,
1992); the invasion of the ctenophore Mnemiopsis leidyi fram the
eastern coast of North America to the Black Sea resulting in
modifications of the plankton and elimination of some otherwise
profitable fisheries (Harbison, 1993). Movements over small distances
can also result in serious consequences as in the case of Gyrodactylus
transferred from the Baltic Sea to Norway with salmon, Salmo salar.
•
Where little consideration is given to ecological consequences, in the"
movement of exotic species associated with shellfish movements, serious
biological consequences may be expected. The movement of half-grown
Pacific oysters from France to Ireland has presently been suspended
pending further discussion .
.,
, ACKNOWLEDGEMENTS
We would like to acknowledge the assistance of Prof. Inger Wallentinus.
Drs Eric Edwards and Peter Dare for information readily provided.
.
REFERENCES
Bernard, F.R., 1969. The parasitic copepod Mytilicola orientalis in British
Columbia Bivalves.
Journal of the Fisheries Research Board of Canada 26:
190-191.
Blateau, D., Le Coguic, V., Mialhe, E. & Grizel, H., 1992. Mussei
(Mytilus edulis) treatment against the red copepod
. Mytilicola intestinalis.
Aquaculture, 107: 165-169.
Comps, M. Grizel, H., Tige, G., & Duthoit, J-L., 1975. Pathologie des
invertebres.- Parasites nouveaux de la glande digestive
des Mollusques mainis, Mytilus edulis L. et Cardium edule,
L. C.R. Acad. Sc. Paris 281: 179-181.
Critchley, 'Ä.T; & Dijkema, R., 1984. On the presence of the introduced
brown alga Sargassum muticum attached to commercially
imported Ostrea edulis in the S.W. Netherlands.
Botanica Manna 27: 211-216..
Crowley, M., 1972. The parasitology of Irish musseis.
Department of Agriculture and Fisheries, Fishery Leaflet
No. 35., 12pp.
..
Korean J. ZooI., 35: 240-255.
Katkansy, S.C., Sparks, A.K. & Chew, K.K., 1967. Distribution and
effects of the endoparasitic copepod Mytilicola orientalis
on the Pacific oyster Crassostrea gigas.
Proc. Nat. Shellfish. Assoc., 57: 50-58.
Ollaug, T.O., 1946. The effect of the copepod, Mytilicola orientalis upon
the Olympian oyster, Ostrea lurida.
Trans. Am. Microscop., 65: 311-317.
O'Mahony, J.H.T. (1993) Phytolankton Species Associated with
Imports of the Pacific Oyster, from France to Ireland.
ICES C.M. K.
Quiniou, F. & Blanchard, M. 1987. Etat de la proliferation de la crepidule
(Crepidula fornicata L.) dans le secteur de Granville
(Golfe Normano-Breton)-.1985. Haliotus 16: 513-526.
~Minchin,
,
D.; Duggan, C.B. & McGrath, D., 1987. Calyptraea chinensis
(Mollusca: Gastropoda) on the west coast of Ireland: a
case of accidental introduction?
J. Conch., 32(5): 297-302
Nicolas, J.L., Comps, M. & Cochennec, N. 1992. Herpes -like virus
infecting Pacific-oyster larvae, Crassostrea gigas. Sull.
Eur. Ass. Fish Pathol., 12(1): 11.
Piquion, J.-C., 1985. Lutte contre les competiteurs.
Equinox, No. 3 : 27-31.
Snyder, F.L., Garton, D.W. & Brainard, M. 1992. Zebra musseIs in the
Great Lakes: The invasion and its implications. The
. Ohio State University. 4pp
Scagel, R.F., 1956. Introduction of a Japanese alga, Sargassum muticum
into the north-east Pacific.
Fisheries Research papers, Washington Department of
Fisheries 1: 49-59.
Sparks, A.K., 1962. Metaplasia of the gut of the oyster Crassostrea
gigas (Thunberg) caused by infection with the copepod
Mytilicola orientalis Mori.
J. Insect Pathol., 4(4): 57-62.
Theisen, B.F., 1987. Mytilicola intestinalis Steuer and the condition of its
host Mytilus edulis L.
Ophelia 27(2): 77-86.
Tige, G., & Rabouin, M.A~, 1976. Etude d'un lot de moules transferees
dans un centre touche par I'epizootie affectuant I'hiutre
plate.I.C.E.S. C.M. 1976/K:21 Shellfish Committee.
Yamauchi, K., 1984. The formation of Sargassum beds on artificial
substrata by transplanting seedlings of S. horneri (Turner)
c. Agardh and S. muticum (Yendo) Fensholt.
Bulletin of the Japanese Society of Scientific Fisheries 50
(7): 1115-1123.
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Table 1. Importations of Pacific oyster, C. gigas, from France to Ireland during 1993 with associated organisms.
* indicates oysters from a nursery system. + removed from the sea soon after introduction.' Oysters from the f
first introduction to Carlingford had 2.7% to 5.3% infestation of M. orientalis on 10 March 1993, local
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populations had none.
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Import
date
Area
Relaycd
Source
23-1-93
4-2-93
5-2-93
19-2-93
25·2·93
25-2-93
26-2-93
4-3-93
5-3-93
6-3-93
19-3-93
23-3-93
25-3-93
4-93
4-93
3/4-93
22-4-93
Carlingford
Carlingford
Dungarvan
Dungarvan
Dungarvan
Cork Harb.+
Carlingford
Dungarvan
SampIe
Dungarvan
Carlingford
Sampie *
Dungarvan
Sampie
Oysterhaven
Dunmanus
Dungarvan
Marennes
Marennes
Normandy
Normandy
Marennes
Marennes
Marennes
Normandy
Arcachon
Normandy
Marennes
Normandy
lrishIBritish
Normandy
Arcachon
not knowll
Normandy
Quantity
importcd
Examincd
1717kg
4000kg
3300kg
3300kg
5340kg
770kg
9970kg
3300kg
4kg
3300kg
15000kg
2kg
2kg
2kg
yes
no
no
no
yes
yes
ycs
no
yes
no
yes
yes
yes
yes
yes
Number
withM.
ostrea
present
SampIe
sizc
Ostrea
edulis
Crepidula
fornicata
SampIe
size
%withM
orientalist
113
0
1
86
7.3
308
5
1
0
67
23
82
14.9
4.3
9.7
?
1721
0
0
80
3.7
3
138
46
68
230
60
0
0
0
0
0
0
0
30
46
68
60
40
0
30.3
0
0
0
0
0
0
6.6
5
I.
,
"\ >.;
..
1·I'i"
5
0
80
0
. :.,!
2
1
"
J
HO
3,000,000
" spat (0.5kg)
ycs
present
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.. IRELAND
Y
. Areas in which C. gigas fram France were reJaid.
My ti licola
0 r i en ta lis
. found in C.gigas fram Arcachan.Marenne/Oleronn
, and St. Vaast Ja Hougue (Narmandy):